Interhemispheric Effect of Parietal TMS on Somatosensory Response Confirmed Directly with Concurrent TMS–fMRI

Transcranial magnetic stimulation (TMS) has been used to document some apparent interhemispheric influences behaviorally, with TMS over the right parietal cortex reported to enhance processing of touch for the ipsilateral right hand (Seyal et al., 1995). However, the neural bases of such apparent interhemispheric influences from TMS remain unknown. Here, we studied this directly by combining TMS with concurrent functional magnetic resonance imaging (fMRI). We applied bursts of 10 Hz TMS over right parietal cortex, at a high or low intensity, during two sensory contexts: either without any other stimulation, or while participants received median nerve stimulation to the right wrist, which projects to left primary somatosensory cortex (SI). TMS to right parietal cortex affected the blood oxygenation level-dependent signal in left SI, with high- versus low-intensity TMS increasing the left SI signal during right-wrist somatosensory input, but decreasing this in the absence of somatosensory input. This state-dependent modulation of SI by parietal TMS over the other hemisphere was accompanied by a related pattern of TMS-induced influences in the thalamus, as revealed by region-of-interest analyses. A behavioral experiment confirmed that the same right parietal TMS protocol of 10 Hz bursts led to enhanced detection of perithreshold electrical stimulation of the right median nerve, which is initially processed in left SI. Our results confirm directly that TMS over right parietal cortex can affect processing in left SI of the other hemisphere, with rivalrous effects (possibly transcallosal) arising in the absence of somatosensory input, but facilitatory effects (possibly involving thalamic circuitry) in the presence of driving somatosensory input.

[1]  M. Calford,et al.  Interhemispheric transfer of plasticity in the cerebral cortex. , 1990, Science.

[2]  R. Deichmann,et al.  Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. , 2008, Cerebral cortex.

[3]  V. Raos,et al.  Crosstalk between the two sides of the thalamus through the reticular nucleus: A retrograde and anterograde tracing study in the rat , 1993, The Journal of comparative neurology.

[4]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[5]  C. L. Kwan,et al.  Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. , 1998, Journal of neurophysiology.

[6]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[7]  P M Rossini,et al.  Left frontal transcranial magnetic stimulation reduces contralesional extinction in patients with unilateral right brain damage. , 1999, Brain : a journal of neurology.

[8]  D. Kleinfeld,et al.  Suppressed Neuronal Activity and Concurrent Arteriolar Vasoconstriction May Explain Negative Blood Oxygenation Level-Dependent Signal , 2007, The Journal of Neuroscience.

[9]  S. P. Richardson,et al.  Crossed Inhibition of Sensory Cortex by 0.3 Hz Transcranial Magnetic Stimulation of Motor Cortex , 2005 .

[10]  M. Calford,et al.  Interhemispheric modulation of somatosensory receptive fields: evidence for plasticity in primary somatosensory cortex. , 1996, Cerebral cortex.

[11]  A. Iriki,et al.  Book Review: Bilateral Activity and Callosal Connections in the Somatosensory Cortex , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[12]  Riitta Hari,et al.  Improved differentiation of tactile activations in human secondary somatosensory cortex and thalamus using cardiac-triggered fMRI , 2006, Experimental Brain Research.

[13]  Felix Blankenburg,et al.  Concurrent TMS and fMRI: Methods and Current Advances , 2008 .

[14]  Riitta Hari,et al.  Transient Suppression of Ipsilateral Primary Somatosensory Cortex during Tactile Finger Stimulation , 2006, The Journal of Neuroscience.

[15]  P. Haggard,et al.  Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. , 2008, Cerebral cortex.

[16]  Akitake Kanno,et al.  Ipsilateral Area 3b Responses to Median Nerve Somatosensory Stimulation , 2003, NeuroImage.

[17]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[18]  G. Vallar,et al.  Spatial frames of reference and somatosensory processing: a neuropsychological perspective. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[20]  Y. Iwamura,et al.  Bilateral receptive field neurons and callosal connections in the somatosensory cortex. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  J. Hahm,et al.  Cortically induced thalamic plasticity in the primate somatosensory system , 1998, Nature Neuroscience.

[22]  S Noachtar,et al.  Ipsilateral median somatosensory evoked potentials recorded from human somatosensory cortex. , 1997, Electroencephalography and clinical neurophysiology.

[23]  Jon Driver,et al.  Neural correlates of crossmodal visual-tactile extinction and of tactile awareness revealed by fMRI in a right-hemisphere stroke patient , 2006, Neuropsychologia.

[24]  Á. Pascual-Leone,et al.  Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex , 2001, Nature Neuroscience.

[25]  B. Christensen,et al.  The mechanisms of interhemispheric inhibition in the human motor cortex , 2002, The Journal of physiology.

[26]  Sandra E. Black,et al.  Task-Relevant Modulation of Contralateral and Ipsilateral Primary Somatosensory Cortex and the Role of a Prefrontal-Cortical Sensory Gating System , 2002, NeuroImage.

[27]  Takeo Ishigaki,et al.  Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation—an fMRI study , 2005, Clinical Neurophysiology.

[28]  F. Ebner,et al.  Chronic suppression of activity in barrel field cortex downregulates sensory responses in contralateral barrel field cortex. , 2005, Journal of neurophysiology.

[29]  R. Spreafico,et al.  A reticuloreticular commissural pathway in the rat thalamus , 1994, The Journal of comparative neurology.

[30]  M Seyal,et al.  Increased sensitivity to ipsilateral cutaneous stimuli following transcranial magnetic stimulation of the parietal lobe , 1995, Annals of neurology.

[31]  Mark Tommerdahl,et al.  Ipsilateral Input Modifies the Primary Somatosensory Cortex Response to Contralateral Skin Flutter , 2006, The Journal of Neuroscience.

[32]  Y. Samson,et al.  Somatosensory cortical activations are suppressed in patients with tactile extinction , 1999, Neurology.

[33]  P M Rossini,et al.  Interhemispheric asymmetries in the perception of unimanual and bimanual cutaneous stimuli. A study using transcranial magnetic stimulation. , 1999, Brain : a journal of neurology.

[34]  M. Kinsbourne Hemi-neglect and hemisphere rivalry. , 1977, Advances in neurology.

[35]  M. Seyal,et al.  Suppression of spatial localization of a cutaneous stimulus following transcranial magnetic pulse stimulation of the sensorimotor cortex. , 1997, Electroencephalography and clinical neurophysiology.

[36]  Carsten Klingner,et al.  Behavioral correlates of negative BOLD signal changes in the primary somatosensory cortex , 2008, NeuroImage.

[37]  J. Kaas,et al.  The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys , 1983, The Journal of comparative neurology.

[38]  G. Curio,et al.  Imperceptible Stimuli and Sensory Processing Impediment , 2003, Science.

[39]  V. Raos,et al.  Connections of the thalamic reticular nucleus with the contralateral thalamus in the rat , 1992, Neuroscience Letters.

[40]  T. Carpenter,et al.  Linear coupling between functional magnetic resonance imaging and evoked potential amplitude in human somatosensory cortex , 2000, Neuroscience.

[41]  a.R.V.,et al.  Clinical neurophysiology , 1961, Neurology.

[42]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[43]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[44]  Ingo G. Meister,et al.  Interhemispheric imbalance during visuospatial attention investigated by unilateral and bilateral TMS over human parietal cortices , 2006, Brain Research.

[45]  T. Kaminaga,et al.  Neural consequences of somatosensory extinction: an fMRI study. , 2005, Journal of neurology.

[46]  L. Merabet,et al.  Visual Phosphene Perception Modulated by Subthreshold Crossmodal Sensory Stimulation , 2007, The Journal of Neuroscience.